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The Force for Poleward Chromosome Motion in Haemanthus Cells Acts

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The Force for Poleward Chromosome Motion in Haemanthus Cells Acts The Force for Poleward Chromosome Motion in Haemanthus Cells Acts along the Length of the Chromosome during Metaphase but Only at the Kinetochore during Anaphase Alexey Khodjakov,* Richard W. Cole,* Andrew S. Bajer, ~ and Conly L. Rieder** *Laboratory of Cell Regulation, Wadsworth Center for Laboratories and Research, Albany, New York 12201-0509; ~Department of Biomedical Sciences, State University of New York, Albany, New York 12222; and§Department of Biology, University of Oregon, Eugene, Oregon 97403 Abstract. The force for poleward chromosome motion other force that now transported the fragments to the during mitosis is thought to act, in all higher organisms, spindle equator at 1.5-2.0 tzm/min. These fragments exclusively through the kinetochore. We have used then remained near the spindle midzone until phrag- time-lapse, video-enhanced, differential interference moplast development, at which time they were again contrast light microscopy to determine the behavior of transported randomly poleward but now at ~3/xm/min. kinetochore-free "acentric" chromosome fragments This behavior of acentric chromosome fragments on and "monocentric" chromosomes containing one kine- anastral plant spindles differs from that reported for tochore, created at various stages of mitosis in living the astral spindles of vertebrate cells, and demonstrates higher plant (Haemanthus) cells by laser microsurgery. that in forming plant spindles, a force for poleward Acentric fragments and monocentric chromosomes chromosome motion is generated independent of the generated during spindle formation and metaphase kinetochore. The data further suggest that the three both moved towards the closest spindle pole at a rate stages of non-kinetochore chromosome transport we (~1.0 txm/min) similar to the poleward motion of observed are all mediated by the spindle microtubules. anaphase chromosomes. This poleward transport of Finally, our findings reveal that there are fundamental chromosome fragments ceased near the onset of differences between the transport properties of forming anaphase and was replaced, near midanaphase, by an- mitotic spindles in plants and vertebrates. URING mitosis the two sister kinetochores on each force is produced by kinetochore-associated molecular replicated chromosome acquire a bundle of mi- motors (for review see Mclntosh and Pfarr, 1991; Sawin crotubules (Mt), 1 known as a kinetochore fiber, and Endow, 1993; Rieder and Salmon, 1994) acting on ki- that securely tethers them to opposing spindle poles (for netochore Mts, which themselves are coordinately disas- review see Salmon, 1989; Rieder, 1990). These kineto- sembling within the kinetochore (for review see Mitchison chore fibers are required for producing the forces that and Salmon, 1992; Desai and Mitchison, 1995). move chromosomes poleward throughout mitosis and, as a In animal somatic cells the equatorial alignment of chro- result, all current models envision that the poleward force mosomes on the forming spindle also appears to involve on a chromosome acts exclusively on the kinetochore (for another force that acts on the chromosome arms to coun- review see Mitchison, 1989; McIntosh and Hering, 1991; terbalance the sister kinetochore-based poleward-directed Ault and Rieder, 1994; Inoue and Salmon, 1995). Cur- forces (for review see Rieder and Salmon, 1994; Cassi- rently, the most popular mechanism envisions that this meris et al., 1994; Fuller, 1995). This force, referred to as the polar ejection force or "polar wind," transports chro- mosome arms away from the closest pole during spindle formation (i.e., prometaphase). The presence of this ejec- Address all correspondence to Conly L. Rieder, Laboratory of Cell Regu- tion force can be easily demonstrated by severing chromo- lation, Wadsworth Center for Laboratories and Research, P.O. Box 509, some arms from the kinetochore region with a laser micro- Albany, NY 12201-0509. Tel.: (518) 474-6774. Fax: (518) 486-4901. e-mail: beam during prometaphase. Under this condition the [email protected]. kinetochore-free (acentric) chromosome fragments (ACF) 1. Abbreviations used in this paper: ACF, acentric chromosome fragment; are transported away from the closest pole at ,'-~2 ixm/min Mt, microtubule. (Rieder et al., 1986; Rieder and Salmon, 1994). © The Rockefeller University Press, 0021-9525/96/03/1093/12 $2.00 The Journal of Cell Biology, Volume 132, Number 6, March 1996 1093-1104 1093 The molecular mechanism behind the polar ejection that there are fundamental differences in how chromo- force is unknown. The most popular hypothesis is that somes become positioned on the forming mitotic spindle chromosome arms contain Mt plus-end motors that inter- in plant and animal cells. act with astral and half-spindle Mts growing from the pole (Salmon, 1989; Ault et al., 1991; Carpenter, 1991). This hy- pothesis is supported circumstantially by Wang and Adler's Materials and Methods (1995) recent finding that chromosome arms in chick cells become decorated with a kinesin-like molecule (chromo- Endosperm Preparation kinesin) as the cell enters mitosis. It is also supported by functional studies in Drosophila (Afshar et al., 1995; Mur- Endosperm from the African blood lily, Haemanthus katherinae Bak, were extruded onto agar-coated coverslips and mounted for live cell time- phy and Karpen, 1995) and Xenopus (Vernos et al., 1995) lapse video microscopy as described by Bajer and Mol~-Bajer (1986). that implicate chromosome-associated kinesin-like pro- Some preparations were fixed and stained for the immunogold localiza- teins (NOD and Xklp 1) in chromosome positioning on tion of spindle microtubules by light microscopy as described by De Mey the meiotic (oocyte) spindle. Alternatively, the fact that et al. (1982). the strength of the ejection force is related to Mt density, and depends on the normal behavior of Mt plus ends, sug- Laser Microsurgery and Video-enhancedMicroscopy gests that it arises from the constant growth of dynamically unstable polar-nucleated Mt ends as they impact and push The differential interference contrast video-enhanced light microscopic/ on the chromosome (Ault et al., 1991; Cassimeris et al., laser microsurgery system, described in detail by Cole et al. (1995), was used to sever chromosome arms and to follow their behavior in living 1994; Rieder and Salmon, 1994). Haemanthus endosperm cells. This system is centered around an inverted An important consideration in mitosis research is the differential interference contrast light microscope (Diaphot 200; Nikon extent to which mechanistic findings in one system are ap- Inc., Garden City, NY) equipped with a motorized stage (Ludl MAC plicable to other systems (Rieder et al., 1993). In this re- 2000; Ludl Electronics, Ltd., Hawthorne, NY). In brief, Haemanthus cells were followed with heat-filtered and shuttered 546-nm light using a ×60 gard it is currently unknown whether the polar ejection 1.4 NA differential interference contrast objective and a 0.85 NA con- force is a feature only of the astral mitosis of vertebrate denser. Sequential images were obtained every 4 s by integrating two cells, or whether it is also present during spindle formation video frames directly onto a chip (P100 CCD; Paultek, Princeton, NJ). in other cell types or organisms. Included here are the as- This integrated frame was then routed through Image I (Universal Imag- tral meiotic spindles of animal spermatocytes and the ing Corp., West Chester, PA) for image processing before storage on a la- ser videodisk recorder (LVR-3300M; Sony Corp. of America, Montvale, anastral spindles of many animal oocytes (e.g., mouse, NJ). Electronic and optical noise within the system was reduced by back- Drosophila, Xenopus) and most plants. Unlike astral spin- ground subtraction and by recording an eight-frame jumping average. dies, which are formed from two radial (astral) arrays of The chromosome microsurgery system used in our study was based on centrosomal Mts, the anastral spindles of some oocytes a pulsed (5 ns) Neodymium-YAG (yttrium-aluminum-garnet) laser (Sure- lite II; Continuum, Santa Clara, CA). The 1064-rim output of this laser and higher plants are organized primarily by the chromo- was frequency doubled to 532 nm and filtered to remove stray 1064-nm somes from random Mt arrays (for review see Smirnova light. This beam was then steered into the epiport of the Diaphot 200 and Bajer, 1992; Rieder et al., 1993; Vernos and Karsenti, where it was reflected, via a custom-made dichroic mirror (Omega Opti- 1995). Since forming anastral spindles lack well-developed cal, Brattleboro, VT), through the Wollaston prism and onto the back ap- arrays of polar Mrs, and since the polar ejection force has erture of the 1.4 NA objective. The objective then focused the beam to a diffraction-limited spot of ~0.5qxm diam (Cole et al., 1995). As demon- only been demonstrated for spindles formed from astral strated by Berns and others (for review see Berns et al., 1991; Cole et al., Mt arrays, it is possible that these two distinct pathways of 1995; Rieder et al., 1995), pulsed 532-nm laser light can be used to selec- spindle morphogenesis produce spindles that utilize fun- tively destroy chromatin and chromatin-associated organelles (e.g., kine- damentally different mechanisms to position chromo- tochores, nucleolar organizers) in living mitotic cells without deleteriously affecting spindle Mts or the process of mitosis. somes, i.e., that astral and anastral spindles exert different The focused laser spot at the specimen plane was set near the center of non-kinetochore-based forces on the chromosomes. a video screen, and its exact position was determined by irradiating a To evaluate this possibility, we have examined the be- dried film of RBC5. Once located, the position of the laser was marked havior of ACFs and monocentric chromosomes containing with cross-hairs on the video monitor. Cutting was then achieved by using a single kinetochore, created at various stages of mitosis the Ludl motorized stage to slowly pass the specimen through the fixed la- ser beam path. In our system optimal chromosome cutting was achieved by laser microsurgery in Haemanthus endosperm.
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